Bone Loss and Patterns of Bone Destruction

Fermin A. Carranza, Paulo M. Camargo and Henry H. Takei

Although periodontitis is an infectious disease of the gingival tissue, changes that occur in bone are crucial, because the destruction of bone is responsible for tooth loss.

The height and density of the alveolar bone are normally maintained by an equilibrium, regulated by local and systemic influences, between bone formation and bone resorption.12,14 When resorption exceeds formation, both bone height and bone density may be reduced (see Video 21-1: Vertical Bone Loss).

The level of bone is the consequence of past pathologic experiences, whereas changes in the soft tissue of the pocket wall reflect the present inflammatory condition. Therefore, the degree of bone loss is not necessarily correlated with the depth of periodontal pockets, the severity of ulceration of the pocket wall, or the presence or absence of pus.

Bone Destruction Caused by the Extension of Gingival Inflammation

The most common cause of bone destruction in periodontal disease is the extension of inflammation from the marginal gingiva into the supporting periodontal tissues. The inflammatory invasion of the bone surface and the initial bone loss that follows mark the transition from gingivitis to periodontitis.

Periodontitis is always preceded by gingivitis, but not all gingivitis progresses to periodontitis. Some cases of gingivitis apparently never become periodontitis, and other cases go through a brief gingivitis phase and rapidly develop into periodontitis. The factors that are responsible for the extension of inflammation to the supporting structures, thereby initiating the conversion of gingivitis to periodontitis, are not clearly understood at this time.

The transition from gingivitis to periodontitis is associated with changes in the composition of bacterial plaque. In advanced stages of disease, the number of motile organisms and spirochetes increases, whereas the number of coccoid rods and straight rods decreases.³⁴ The cellular composition of the infiltrated connective tissue also changes with increasing severity of the lesion (see Chapter 7). Fibroblasts and lymphocytes predominate in stage 1 gingivitis, whereas the number of plasma cells and blast cells increases gradually as the disease progresses. Seymour and colleagues^58,59 have postulated a stage of “contained” gingivitis in which T lymphocytes are preponderant; they think that, as the lesion becomes a B-lymphocyte lesion, it becomes progressively destructive.

Heijl and coworkers ²² were able to convert, in experimental animals, a confined, naturally occurring chronic gingivitis into a progressive periodontitis by placing a silk ligature into the sulcus and tying it around the neck of the tooth. This induced ulceration of the sulcular epithelium, a shift in the inflammatory infiltrate from predominantly plasma cells to predominantly polymorphonuclear leukocytes, and osteoclastic resorption of the alveolar crest. The recurrence of episodes of acute destruction over time may be one mechanism that leads to progressive bone loss in individuals with marginal periodontitis.

The extension of inflammation to the supporting structures of a tooth may be modified by the pathogenic potential of plaque and the resistance of the host. The latter includes immunologic activity and other tissue-related mechanisms, such as the degree of fibrosis of the gingiva, probably the width of the attached gingiva, and the reactive fibrogenesis and osteogenesis that occur peripheral to the inflammatory lesion.⁵²

Histopathology.

Gingival inflammation extends along the collagen fiber bundles and follows the course of the blood vessels through the loosely arranged tissues around them into the alveolar bone ⁶⁷ (Figure 21-1). Although the inflammatory infiltrate is concentrated in the marginal periodontium, the reaction is a much more diffuse one, often reaching the bone and eliciting a response before evidence of crestal resorption or loss of attachment exists.⁴¹ In the upper molar region, inflammation can extend to the maxillary sinus, thereby resulting in thickening of the sinus mucosa.⁴⁰

Figure 21-1 A, An area of inflammation extending from the gingiva into the suprabony area. B, Extension of inflammation along the blood vessels and between collagen bundles.

Interproximally, inflammation spreads to the loose connective tissue around the blood vessels, through the fibers, and then into the bone through vessel channels that perforate the crest of the interdental septum at the center of the crest (Figure 21-2), toward the side of the crest (Figure 21-3), or at the angle of the septum. In addition, inflammation may enter the bone through more than one channel. Less frequently, the inflammation spreads from the gingiva directly into the periodontal ligament and from there into the interdental septum¹ (Figure 21-4).

Figure 21-2 Inflammation that extends from the pocket area *(top)* between the collagen fibers, which are partially destroyed.

Figure 21-3 A, Extension of inflammation into the center of the interdental septum. Inflammation from the gingiva penetrates the transseptal fibers and enters the bone around the blood vessel in the center of the septum. B, The cortical layer at the top of the septum has been destroyed, and the inflammation penetrates into the marrow spaces.

Figure 21-4 Pathways of inflammation from the gingiva into the supporting periodontal tissues in a patient with periodontitis. A, Interproximally, from the gingiva into the bone *(1),* from the bone into the periodontal ligament *(2),* and from the gingiva into the periodontal ligament *(3).* B, Facially and lingually, from the gingiva along the outer periosteum *(1),* from the periosteum into the bone *(2),* and from the gingiva into the periodontal ligament *(3).*

Facially and lingually, inflammation from the gingiva spreads along the outer periosteal surface of the bone (see Figure 21-4) and penetrates into the marrow spaces through vessel channels in the outer cortex.

Along its course from the gingiva to the bone, the inflammation destroys the gingival and transseptal fibers, reducing them to disorganized granular fragments interspersed among the inflammatory cells and edema.⁴⁵ However, there is a continuous tendency to recreate transseptal fibers across the crest of the interdental septum farther along the root as the bone destruction progresses (Figure 21-5). As a result, transseptal fibers are present, even in cases of extreme periodontal bone loss.

Figure 21-5 Reformation of transseptal fibers. A mesiodistal section through the interdental septum shows gingival inflammation and bone loss. Recreated transseptal fibers can be seen above the bone margin, where they have been partially infiltrated by the inflammatory process.

The dense transseptal fibers form a firm covering over the bone that is encountered during periodontal flap surgery after the superficial granulation tissue is removed.⁵⁰

After inflammation reaches the bone via extension from the gingiva (Figure 21-6), it spreads into the marrow spaces and replaces the marrow with a leukocytic and fluid exudate, new blood vessels, and proliferating fibroblasts (Figure 21-7). Multinuclear osteoclasts and mononuclear phagocytes increase in number, and the bone surfaces appear to be lined with Howship lacunae (Figure 21-8).

Figure 21-6 Extension of inflammation has reached the crestal bone surface.

Figure 21-7 Interdental septum in a human autopsy section. Extensive inflammatory infiltrate has invaded the marrow spaces, entering from both the mesial and distal aspects. Fatty bone marrow has been replaced by inflammatory cells and fibrous marrow.

Figure 21-8 Osteoclasts and Howship lacunae in the resorption of crestal bone.

In the marrow spaces, resorption proceeds from within and causes a thinning of the surrounding bony trabeculae and an enlargement of the marrow spaces; this is followed by the destruction of the bone and a reduction in bone height. Normally, fatty bone marrow is partially or totally replaced by a fibrous type of marrow in the vicinity of the resorption.

Bone destruction in periodontal disease is not a process of bone necrosis.²⁷ It involves the activity of living cells along viable bone. When tissue necrosis and pus are present in periodontal disease, they occur in the soft-tissue walls of periodontal pockets rather than along the resorbing margin of the underlying bone.

The amount of inflammatory infiltrate correlates with the degree of bone loss but not with the number of osteoclasts. However, the distance from the apical border of the inflammatory infiltrate to the alveolar bone crest correlates with both the number of osteoclasts on the alveolar crest and the total number of osteoclasts.⁵¹ Similar findings have been reported in experimentally induced periodontitis in animals.³²

Radius of Action

Garant and Cho ¹⁰ suggested that locally produced bone resorption factors may need to be present in the proximity of the bone surface to exert their action. Page and Schroeder,⁴⁹ on the basis of Waerhaug’s measurements made on human autopsy specimens,^64,65 postulated a range of effectiveness of about 1.5 mm to 2.5 mm in which bacterial plaque can induce loss of bone. Beyond 2.5 mm, there is no effect; interproximal angular defects can appear only in spaces that are wider than 2.5 mm, because narrower spaces would be destroyed entirely. Tal⁶¹ corroborated this with measurements in human patients.

Large defects that greatly exceed a distance of 2.5 mm from the tooth surface (as described in aggressive types of periodontitis) may be caused by the presence of bacteria in the tissues.6,10,54

Rate of Bone Loss

In a study of Sri Lankan tea laborers with no oral hygiene and no dental care, Löe and colleagues ³⁶ found the rate of bone loss to average about 0.2 mm per year for facial surfaces and about 0.3 mm per year for proximal surfaces when periodontal disease was allowed to progress untreated. However, the rate of bone loss may vary, depending on the type of disease present. Löe and colleagues³⁵ also identified the following three subgroups of patients with periodontal disease on the basis of the interproximal loss of attachment and tooth mortality (loss of attachment can be equated with loss of bone, although attachment loss precedes bone loss by about 6 to 8 months¹⁷):

1. Approximately 8% of persons had a rapid progression of periodontal disease that was characterized by a yearly loss of attachment of 0.1 mm to 1.0 mm.

2. Approximately 81% of individuals had moderately progressive periodontal disease with a yearly loss of attachment of 0.05 mm to 0.5 mm.

3. The remaining 11% of persons had minimal or no progression of destructive disease with a yearly loss of attachment of 0.05 mm to 0.09 mm.

Periods of Destruction

Periodontal destruction occurs in an episodic, intermittent manner, with periods of inactivity or quiescence that alternate with destructive periods that result in the loss of collagen and alveolar bone and the deepening of the periodontal pocket.

Periods of destructive activity are associated with subgingival ulceration and an acute inflammatory reaction that results in the rapid loss of alveolar bone 49,56; it has been hypothesized that this coincides with the conversion of a predominantly T-lymphocyte lesion to one with a predominantly B-lymphocyte–plasma cell infiltrate.⁵⁹ Microbiologically, these lesions are associated with an increase in the loose, unattached, motile, gram-negative, anaerobic pocket flora, whereas periods of remission coincide with the formation of a dense, unattached, nonmotile, gram-positive flora with a tendency to mineralize.⁴³

It has also been suggested that the onset of periods of destruction coincide with tissue invasion by one or several bacterial species and that this is followed by an advanced local host defense that controls the attack.⁵⁴

Mechanisms of Bone Destruction

The factors involved in bone destruction in periodontal disease are bacterial and host mediated. Bacterial plaque products induce the differentiation of bone progenitor cells into osteoclasts and stimulate gingival cells to release mediators that have the same effect.21,57 Plaque products and inflammatory mediators can also act directly on osteoblasts or their progenitors, thereby inhibiting their action and reducing their numbers.

In addition, in patients with rapidly progressing diseases (e.g., aggressive periodontitis), bacterial microcolonies or single bacterial cells have been found between collagen fibers and over the bone surface, which suggests a direct effect.6,9,57

Several host factors released by inflammatory cells are capable of inducing bone resorption in vitro, and they play a role in periodontal disease. These include host-produced prostaglandins and their precursors, interleukin-1α, interleukin-β, and tumor necrosis factor-α.

When injected intradermally, prostaglandin E₂ induces the vascular changes that are seen with inflammation; when injected over a bone surface, prostaglandin E₂ induces bone resorption in the absence of inflammatory cells, with few multinucleated osteoclasts.18,26 In addition, nonsteroidal anti-inflammatory drugs (e.g., flurbiprofen, ibuprofen) inhibit prostaglandin E₂ production, thereby slowing bone loss in naturally occurring periodontal disease in beagle dogs and humans. This effect occurs without changes in gingival inflammation, and it rebounds 6 months after the cessation of drug administration.^25,68 (For more information about the host-mediated mechanisms of bone destruction, see Chapter 25.)